Repeated genetic adaptation under demographic limits in kiwifruit

Population genetic theory predicts that species with narrow geographic distributions experience stronger genetic drift, higher inbreeding, and greater mutational burden than their widespread relatives, yet how demographic history shapes the genomic basis of adaptation remains poorly understood. We hypothesized that (i) restricted-range species exhibit reduced genetic diversity, elevated inbreeding, and greater mutation load owing to smaller long-term effective population sizes; (ii) despite these demographic constraints, shared environmental pressures can still drive repeated adaptation; (iii) repeated adaptation may arise through ancestral standing genetic variation, adaptive introgression, or independent de novo mutations. We tested these hypotheses using two kiwifruit species, Actinidia hemsleyana (narrow-ranged) and Actinidia eriantha (widespread), which differ markedly in demographic history and range size but occupy overlapping environments in subtropical China. We show that demographic contraction and inbreeding have eroded genome-wide diversity in the range-restricted species, accompanied by a substantially higher load of deleterious mutations. Despite these contrasting demographic legacies, both species exhibit repeated genomic responses to shared climatic gradients, with adaptation targeting similar genes. Such repeated adaptation was driven primarily by ancestral standing variation, with smaller contributions from adaptive introgression and only limited evidence for independent de novo mutations. These results reveal that demographic constraints shape genome-wide diversity and mutation load but do not preclude repeated adaptation when shared genetic variation remains available.